Tri-RNAseq of a biocontrol agent and a pathogenic fungus during interaction with the host

Biocontrol strategies offer a promising alternative to control plant pathogens achieving food safety and food security. The aim of this study was to decipher the molecular interactions involving the biocontrol agent (BCA) yeast Papiliotrema terrestris strain PT22AV, the postharvest pathogen Penicillium expansum, and the host Malus domestica. RNAseq analysis was performed to identify the differentially expressed genes of the BCA, the pathogen, and the host during both their respective dual and tritrophic interactions. Analysis of transcriptome changes in the BCA revealed overexpression of genes involved in nutrients uptake and oxidative stress response, regardless of the presence of the pathogen. This suggests that these processes are crucial for the BCA to rapidly colonize the ecological niche (fruit wounds) and outcompete the pathogen. In the absence of P. expansum, BCA genes involved in metabolism and transport of carbohydrates were highly represented, suggesting a different nutritional requirement of P. terrestris PT22AV when it is not competing with the pathogen. As to transcriptomic analysis of P. expansum, genes involved in transcription, oxidation reduction process, transmembrane transport, and amine and peptide metabolism were the most represented GO categories, regardless of the presence of the BCA. While in the absence of the BCA there was only enrichment of oxidation reduction process, in its presence metabolic processes of polysaccharides, aminoglycan and glucosamine-containing compounds were strongly enriched, suggesting a substantial nutritional rewiring of the pathogen to directly outcompete the BCA. Analysis of the transcriptomic changes of the host M. domestica revealed overexpression of genes involved in host defense signaling pathways in the presence of both the BCA and the pathogen, and a prevalence of PTI and ETI host genes activated during interaction with P. expansum only. This analysis contributes to advance the knowledge on the molecular mechanisms that underlie biocontrol activity and the tritrophic interaction of the BCA with the pathogen and the host.